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Antiretroviral Therapy and COVID-19 Interaction Outcomes in HIV- Positive Patients

Rabaa Y athamnehˡ , Abdelrahim Alqudah2 , Rawan Abudalo2, Murat Sayan³’⁴, Ayse Arikanˡ’⁴

ˡNear East University, Faculty of Medicine, Medical Microbiology and Clinical Microbiology, Nicosia, Northern Cyprus.

² Department of Clinical Pharmacy and Pharmacy Practice, Faculty of Pharmaceutical Sciences, The Hashemite University, P.O box 330127, Zarqa 13133 Jordan

³Kocaeli University, Faculty of Medicine, Clinical Laboratory, PCR Unit, Kocaeli, Turkey

⁴Near East University, DESAM Institute, Nicosia, Northern Cyprus

3Jordanian Royal Medical Services, Radiology Department, Amman, Jordan

Corresponding author: RabaaY athamneh, [email protected] ORCID ID: 0000-0001-5447-9385

Abstract

Objectives: COVID-19 is a new serious upper respiratory infectious disease that might be risky on immunodeficient patients, particularly HIV-positive Patients. This review aims to present a better understanding for the current effects of COVID-19 infection on HIV patients and to review the impact of using antiretroviral therapy in patients with COVID-19 infection.

Methods: Pubmed, Google Scholar, Websites were searched for the studies that focus on evaluating the impact of COVID-19 disease among people with HIV and the effects of ARV therapy combined with COVID-19.

Key findings: the studies have proposed that HIV-positive people who are well managed are not under risk of inferior COVID-19 disease outcomes compared to HIV negative people with COVID-19, Furthermore, HIV patients who have undergone a Tenofovir-containing regimen have a lower risk of getting COVID-19 infection and its associated hospitalization compared to those who received other treatments. On the other hand, lopinavir/ darunavir may not be effective against respiratory function deterioration. In addition, the effectiveness of Lopinavir/ritonavir against SARS-CoV-2 or SARS-COV-2 with HIV co-infection was still controversial

Conclusions: Based on the results of the reviewed studies, COVID-19 did not increase morbidity and mortality among HIV-positive individuals, ARV varies in its effectiveness against SARS- CoV-2 among people with HIV, whereas the TDF, TAF, ABC, and FTC had efficacy against SARS-CoV-2,the efficacy of Lopinavir/darunavir or lopinavir/ritonavir against SARS-CoV-2 or SARS-CoV-2 with HIV co-infection was debatable. More evidence is still needed to demonstrate these outcomes.

Keywords: COVID-19, HIV, antiretrovirals

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Background:

The novel Coronavirus Disease 2019 (COVID - 19) as it was officially called by World Health Organization (WHO) is an infection that resulted from severe acute respiratory syndrome Coronavirus 2 (SARS-CoV-2) 1,2, firstly, it has been reported in Wuhan, Hubei Province, China in December 2019 3. Since then, it is promptly extended to more than 200 countries and has been revealed as a pandemic disease by the WHO 4. On June 25, 2021, about 180,844,369 confirmed cases were reported globally of which 165,478,537 cases have recovered and there were officially 3,917,742 deaths were recorded 5.

COVID-19 is considered mostly as a mild illnesses. However, 14 - 26% of those infected people have developed a severe illness that needs hospitalization with oxygen support, and some of those patients may need to be admitted to the intensive care unit 6. In some severe cases, organ dysfunction may be developed, such as progressive respiratory failure, heart, and kidney injuries, which increase the mortality rate in such cases 7,8. In addition, a large body of evidence has revealed that the disease severity and mortality rate are increased in elderly people, or patients with underlying comorbidities such as hypertension, cardiovascular diseases, and diabetes9, in addition to immunodeficient people 10. Since people with human immunodeficiency virus (HIV) suffer from failure in their immune system which is associated with other comorbidities 11, the world's fears have been shifted towards the HIV and COVID-19 interaction outcomes especially in countries with a high percentage of people with HIV such as Africa 12. Globally, by the end of 2019, statistics showed that the sum of people who live with HIV/AIDS is around 38 million 13 for all people were living with HIV, 81% of them know that they are infected, 67% of those who know they are infected receive HIV treatment13. HIV-positive people who have a lower count of CD4 cells have comorbidities, and unsuppressed HIV RNA viral load may be under risk of getting other severe diseases such as COVID-1914,15. Therefore, regular use of antiretroviral therapy (ARV) such as nucleoside reverse transcriptase inhibitors (NRTIs), protease inhibitors (PIs), fusion inhibitors, integrase inhibitors (INSTIs), co-receptor antagonists, or non-nucleoside reversible transport inhibitors (NNRTIs) is essential to improve their health status 16. Besides many research evaluating HIV treatment options for the availability of various antiretroviral combinations and the different properties of each combination 17 Thereby, this review will summarize some clinical presentations of COVID-19 effects on people with HIV and the interaction outcomes of ARV therapy with COVID-19. Methods: Pubmed, Google Scholar, Websites were searched for the studies that focus on evaluating the impact of COVID-19 disease among people with HIV and the effects of ARV therapy combined with COVID-19.

Key Findings:

COVID-19 impacts on HIV-positive people

Centers for Disease Control and Prevention (CDC) have considered individuals who living with HIV as a population that could be at greater risk with COVID-19 infection as opposed to HIV- negative people18. Nevertheless, the relation between COVID-19 and HIV is still indistinct 19. Several studies have shown that individuals with positive HIV and COVID-19 had clinical presentations and effects similar to patients with negative HIV with COVID-19. Furthermore, the

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risk of developing severe diseases in people with COVID-19 and HIV has been appeared as analogous to the overall population12,20,21To date, a variety of drugs and techniques in the therapy of the disease have been used. Nevertheless, there has been no effective therapeutic choice, just successes have so far been achieved based on cases so many studies interested to evaluate the options of COVID-19 treatment22.

A systematic review analysed eight studies to demonstrate the clinical outcomes comorbidities and safety supply of antiretrovirals to HIV positive people who are infected COVID-19. It has shown that HIV-positive people who are well managed are not under risk of inferior COVID-19 disease outcomes compared to HIV-negative people with COVID-19 23. Following the previously mentioned studies, Patel et al. conducted a study about COVID-19 and HIV coinfection cases at New York Medical Centre throughout March and May 2020. This study included 100 people with HIV and 4513 without HIV with median ages of the HIV and non-HIV groups were 62 and 65 years respectively 24. The results of this study showed that the status of HIV had no apparent effect on the odds of death during hospitalization due to COVID-19. The death rate was 22% in people with HIV positive compared to 24% of the HIV negative people, and the length of hospitalization in all groups was 5 days. Besides, there has been no significant difference between the two groups in the frequency of acute kidney injury. Thus, HIV-positive people who were hospitalized with infection of COVID-19 have comparable clinical characteristics and outcomes with HIV-negative patients. Interestingly, the same study showed that people with HIV had an approximately 50% higher risk of intubation 24 which was consistent with other studies showed that HIV positive people had a higher risk of intubation compared to HIV negative people 20,21 which was due to HIV related immunosuppression11. Further studies are urgently needed as consequence to resolve this shortage of data. Another study was performed on a case series for twenty-six HIV positive people who were infected with COVID-19 at Hospital in Italy called S. Orsola throughout March and April 2020 who had median CD4 + lymphocyte count 566 (cells/mm3) and there had been treated by a combination antiretroviral therapy (cART) reported that no patient has been admitted to the intensive care unit and no deaths have occurred 25. Furthermore, the results for this study demonstrated that SARS- CoV-2 infection was not more frequent or more severe among those people, and the associated comorbidities were similar or milder than the general population25.

To interpret the findings of this study, many researchers have hypothesized that HIV positive people who on cART could have a minimal risk of COVID-19 infection and related complications due to the in-vitro efficacy of certain antiretroviral medicines and their lack of cellular immunity, resulting in a reduced risk of cytokine upregulation and serious lung damage

26,27

. On the other hand, another study showed that HIV-positive people had a high risk of COVID-19 infection and mortality compared to HIV-negative individuals due to immune deficiency and chronic inflammation associated with HIV. However, the high mortality is related to the higher comorbidities risk factors in HIV patients. Thus, HIV patients may represent other risk factors where they need special consideration28. Given the fact that HIV can destroy CD4+

cells which play a critical role in immune response coordination, impacting HIV-positive people outcomes, particularly those with a history of advanced diseases 29. Thereby, for a better understanding of the risk and clinical course of COVID-19 among HIV infected people, extended cohort studies are required

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Antiretroviral and COVID-19 interaction outcomes in HIV-positive people

COVID-19 clinical outcomes among HIV-positive patients are still not understood 19,30. On one hand, some studies suggest that HIV-positive patients might be at lower risk of COVID-19 and its associated complications, which could be due to the effect of ARV12. On the other hand, HIV- positive people who are not on antiretroviral or their disease state is not controlled are expected to be at higher risk of COVID-19 infection and its complications or death due to their immune deficiency state 29. Jockusch and his colleagues have conducted molecular research to test the capability of the active triphosphate forms of both tenofovir and emtricitabine to incorporate COVID-19 RNA-dependent RNA polymerase (SARS-CoV-2 RdRp). Tenofovir and emtricitabine are the two elements of emtricitabine/tenofovir alafenamide and emtricitabine/tenofovir disoproxil fumarate the two FDA-approved pre-exposure prophylaxis (PrEP) drugs that are used for HIV infection prevention in people who have not expressed HIV but are still at high risk of HIV infection[30]. This study indicated that tenofovir and emtricitabine triphosphates serve as terminators of the catalyzed SARS-CoV-2 RdRp reaction suggesting a possible benefit of emtricitabine/tenofovir alafenamide and emtricitabine/tenofovir disoproxil fumarate s as PrEP for COVID-1931.

Furthermore, Del Amo et al. have established a cohort study that involved clinics of HIV in sixteen Spanish hospitals from February to April 2020. This study included 77590 HIV positive patients who were 20-79 years of age receiving antiretroviral therapy of both NRTI backbone (emtricitabine (FTC) / tenofovir disoproxil fumarate (TDF), lamivudine (3TC)/abacavir (ABC), tenofovir alafenamide (TAF)/(FTC) or other drugs), and the third medications are PI, INSTI or NNRTI 32. Of the 77,590 individuals with HIV-, 236 had been diagnosed with COVID-19, of which fifteen were entered into the ICU, 151 were hospitalized, and about twenty died. Men and persons were older than 70 years recorded that they were at a high risk of infection with COVID- 19 and hospitalization. The risk of hospitalization per 10 000 people diagnosed with COVID-19 was 20.3% among patients taking TAF/FTC, 10.5% for those who were receiving TDF/FTC, 23.4% among those who were taking ABC/3TC, and 20% for those who received other therapies. None of the patients who received TDF/FTC entered into the intensive care unit or died32. Thereby, people with HIV who received TDF/FTC had been at minimal risk of COVID- 19 hospitalization than those undergoing another therapy. Some molecular research reported the capability of the active triphosphate forms of (TAF) and tenofovir-diphosphate (TFV-DP) for being inhibitors of SARS-CoV-2 RdRp33, whilst another clinical study has shown the capability of active triphosphate forms of both emtricitabine and tenofovir to incorporate SARS-CoV-2 RdRp 31, supporting the effectiveness of nucleotide analogues to lower the risk of COVID-19 in individuals with established HIV.

In addition to inhibition of HIV reverse transcription enzyme, tenofovir has shown immunomodulatory effects in many animals in vitro 34,35 by altering pro-inflammatory cytokines and IL-12 release and reducing monocyte chemoattractant protein 1 (MCP-1), IL-10, and IL-8 production36. This suggests that tenofovir may modulate the overall inflammatory pathways and immune responses against pathogens; thereby it could be an effective treatment against COVID- 19 infection. Further studies are needed to verify tenofovir previous effects.

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Harter et al. conducted a retrospective analysis study that included 33 cases of HIV-positive people with SARS-CoV-2 infection37. This study collected anonymous data related to patient characteristics and other HIV-related parameters (last CD4+ T cells, CD4/CD8 ratio, HIV RNA copies/ml). All patients had been on antiretroviral regimes when they were diagnosed with COVID-19, including NRTIs, PIs, INSTI, and NNRTIs. NRTIs were essentially TAF, TDF, cytidine analog; either FTC, or lamivudine, and darunavir as protease inhibitors 37 In this study, three out of thirty-two patients died (9%) and the percent of recovery was 91%, 76% of which were classified as mild cases. This case series showed that morbidity and mortality outcomes among HIV patients who were managed with antiretroviral therapy were not increased. Thereby, further investigations are required to explain any deleterious or protective impacts of antiretroviral treatment on HIV-positive people diagnosed with COVID-19. A further clinical study reported an effective response of lopinavir/ritonavir against SARS. Lopinavir/ritonavir as PIs are utilized during HIV infection lopinavir is pharmacokinetically improved by booster doses of ritonavir, thereby they are co-formulated38,39

Based on in vivo and in vitro studies, lopinavir/ritonavir has previously been selected as an effective regimen in the field of the SARS and Middle East Respiratory Syndrome (MERS) that caused outbreaks of coronavirus in Asia in 2003 40, and the Middle East/South Korea region in 2012 41,42,43. Thereby, currently, these drugs have been suggested by several studies for SARS- CoV-2 infection treatment44. A retrospective cohort study of 47 mild COVID-19 cases divided into a test group receiving lopinavir/ritonavir therapy with an adjuvant-compared control group that received adjuvant therapy alone.

They have demonstrated a negative PCR conversion time and shorter time to return to the normal body temperature of the lopinavir/ritonavir group compared to the adjuvant therapy control group 45. This suggests the effectiveness of lopinavir/ritonavir addition for COVID-19 infection treatment. In contrast, a randomized controlled open-label study including 199 adults with SARS-CoV-2 infection who were hospitalized, 99 patients of which were being allocated randomly assigned in a 1:1 ratio to get either lopinavir/ritonavir two times per day for fourteen days concomitant with standard care protocol, while 100 patients received the standard care regimen only 44. The study reported no differences in clinical improvement between the studied groups [44]. Thus, the results highlight the need for further clinical studies about lopinavir/ritonavir treatment effectiveness against SARS-COV-2 infection.

Moreover, Riva et al. conducted a study that included three clinical HIV positive reports for two males and one female, aged between 57- 63 who were on an ARV regimen containing darunavir as a PI is given at 800 mg with immunovirological status was rated as good46. After being diagnosed with COVID-19, all cases were hospitalized from March 11 to March 24, 2020, and they have been received the appropriate treatment 46. These clinical reports showed that darunavir had no preventive effect against SARS-CoV-2 infection in HIV-positive people and did not protect against respiratory function worsening 46. Thus, further investigations are still needed to demonstrate the clinical effectiveness of darunavir against respiratory function deterioration in COVID-19 infected patients.

Conversely, on March 9, 2020, Five HIV-positive people have been admitted to the Barcelona Hospital with COVID-19 30 .Four patients with suppressed RNA viral load were on ART regimen. According to their antiretroviral regimen, two patients were on TAF, FTC, and

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darunavir boosted cobicistat regimen, had an upper respiratory infection whilst the other three had viral pneumonia (two patients were on abacavir, lamivudine; and dolutegravir regimen, and one patient with no antiretroviral treatment who is newly diagnosed with HIV), all of the patients have been given boosted protease inhibitor antiretroviral as a treatment after admission. All of them were recovered, and the length of hospitalization for all of them was between 1-21 days.

Two of the patients required ICU entry with invasive and non-invasive mechanical ventilation.

These clinical cases showed that protease inhibitors which were developed to treat HIV, for both lopinavir and darunavir enhanced with ritonavir or cobicistat may not be effectively opposed to acute severe respiratory syndrome caused by SARS-CoV-2 in vivo 30 . Thus, effective treatment or prevention of COVID-19 disease remains a major challenge.

Conclusion

Further studies are urgently needed to

better understand and evaluate the mechanisms of antiretroviral

Further studies are urgently needed to

better understand and evaluate the mechanisms of antiretroviral

Further studies are urgently needed to

better understand and evaluate the mechanisms of antiretroviral

Conclusion:

In conclusion, several studies showed that COVID-19 infection did not increase morbidity and mortality among people with HIV positive, particularly for those under antiretroviral therapy. In addition, some ARVs such as TDF, TAF, ABC, and FTC had efficacy against SARS-CoV-2.

Patients with HIV who received a regimen containing tenofovir could reduce the risk of developing COVID-19 and associated hospitalization. Whereas, lopinavir/darunavir may not be effective against the deterioration of respiratory function which resulted from SARS-CoV-2 infection. In addition, the effectiveness of lopinavir/ritonavir against SARS-CoV-2 or SARS- CoV-2 with HIV co-infection was controversial. More evidence is still needed to demonstrate the clinical effectiveness of ARV based on well-controlled clinical trials.

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“Positive Effects of Covid-19 on Earth.” International Journal of Research in Pharmaceutical Sciences 11, no. “The Hidden Positive Effects of Covid-19

Impact of Liver Test Abnormalities and Chronic Liver Disease on the Clinical Outcomes of Patients Hospitalized with COVID-19 in vidharbha.. region of